Factors Associated with Exclusive Breastfeeding of

Preterm Infants. Results from a Prospective National

Cohort Study
Ragnhild Maastrup
1,2,3
*, Bo Moelholm Hansen
4
, Hanne Kronborg
5
, Susanne Norby Bojesen
3,4
,
Karin Hallum
3,6
, Annemi Frandsen
3,7
, Anne Kyhnaeb
3,8
, Inge Svarer
3,9
, Inger Hallstro m
2
1Knowledge Centre for Breastfeeding Infants with Special Needs at Department of Neonatology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark,
2Department of Health Sciences, Faculty of Medicine, Lund University, Lund, Sweden, 3Danish National Panel of Experts on Breastfeeding Infants with Special Needs,
4Department of Neonatology, Copenhagen University Hospital Herlev, Herlev, Denmark, 5Department of Public Health, Section of Nursing, University of Aarhus, Aarhus,
Denmark, 6Department of Neonatology, Viborg Regional Hospital, Viborg, Denmark, 7Paediatric Department, Holbaek University Hospital, Holbaek, Denmark,
8Department of Neonatology, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark, 9Department of Neonatology, Odense University Hospital, Odense,
Denmark
Abstract
Background and Aim: Evidence-based knowledge of how to guide the mothers of preterm infants in breastfeeding
establishment is contradictive or sparse. The aim was to investigate the associations between pre-specified clinical practices
for facilitating breastfeeding, and exclusive breastfeeding at discharge as well as adequate duration thereof.
Methods: A prospective survey based on questionnaires was conducted with a Danish national cohort, comprised of 1,221
mothers and their 1,488 preterm infants with a gestational age of 2436 weeks. Adjusted for covariates, the pre-specified
clinical practices were analysed by multiple logistic regression analyses.
Results: At discharge 68% of the preterm infants were exclusively breastfed and 17% partially. Test-weighing the infant, and
minimizing the use of a pacifier, showed a protective effect to exclusive breastfeeding at discharge (OR 0.6 (95% CI 0.40.8)
and 0.4 (95% CI 0.30.6), respectively). The use of nipple shields (OR 2.3 (95% CI 1.63.2)) and the initiation of breast milk
expression later than 48 hours postpartum (OR 4.9 (95% CI 1.912.6)) were associated with failure of exclusive breastfeeding
at discharge. The clinical practices associated with an inadequate breastfeeding duration were the initiation of breast milk
expression at 1224 hours (OR 1.6 (95% CI 1.02.4)) and 2448 hours (OR 1.8 (95% CI 1.03.1)) vs. before six hours
postpartum, and the use of nipple shields (OR 1.4 (95% CI 1.11.9)).
Conclusion: Early initiation of breast milk pumping before 12 hours postpartum may increase breastfeeding rates, and it
seems that the use of nipple shields should be restricted. The use of test-weighing and minimizing the use of a pacifier may
promote the establishment of exclusive breastfeeding, but more research is needed regarding adequate support to the
mother when test-weighing is ceased, as more of these mothers ceased exclusive breastfeeding at an early stage after
discharge.
Citation: Maastrup R, Hansen BM, Kronborg H, Bojesen SN, Hallum K, et al. (2014) Factors Associated with Exclusive Breastfeeding of Preterm Infants. Results from
a Prospective National Cohort Study. PLoS ONE 9(2): e89077. doi:10.1371/journal.pone.0089077
Editor: Lynette K. Rogers, The Ohio State Unversity, United States of America
Received August 6, 2013; Accepted January 15, 2014; Published February 19, 2014
Copyright: 2014 Maastrup et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors disclosed receipt of the following financial support for the research and authorship of this article: Funding to support the research was
received from The Swedish Research Council, http://www.vr.se/inenglish.4.12fff4451215cbd83e4800015152.html; Soester Marie Dalgaards Foundation, http://
www.diakonissestiftelsen.dk/Default.aspx?ID=1177; and the Neonatal Department, http://www.rigshospitalet.dk/menu/AFDELINGER/Juliane+Marie+Centret/
Klinikker/Neonatalklinikken/; and the Juliane Marie Centre at Rigshospitalet Copenhagen, http://www.rigshospitalet.dk/menu/AFDELINGER/
Juliane+Marie+Centret/In+English/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: Ragnhild.maastrup@regionh.dk
Background
Breast milk is regarded to be the best nutrition for preterm
infants [1]. However, preterm infants are often not strong enough
to be exclusively breastfed in the first period of their lives.
Therefore the mother is encouraged to start breast milk expression
in order to feed (or supplement) the infant with expressed breast
milk via a feeding tube until such time as it is possible to establish
exclusive breastfeeding [2]. Even though the members of staff in
the Neonatal Intensive Care Units (NICUs) put great effort into
promoting breastfeeding, breastfeeding rates in Danish preterm
infants are significantly lower (65%) at discharge than breastfeed-
ing initiation rates in infants born at term (99%) [3],[4].
The lower breastfeeding rates in preterm infants might partly be
explained by factors associated with preterm birth such as a lower
gestational age (GA), multiple births [5], [6], [7], and maternal
factors like smoking and low socio-economic status (SES) [3], [7],
[8], [9], [10]. These factors are all shown to be negatively related
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to breastfeeding and are, together with previous breastfeeding
experience, circumstances that are known at birth. After delivery a
number of interventions are performed to facilitate breastfeeding.
These are only partly based on evidence and there are significant
differences between the neonatal departments, even in a small
country like Denmark, with regards to clinical practices for the
facilitation of breastfeeding.
Clinical practices to facilitate breastfeeding
A lack of breast milk is one of the greatest barriers for
establishing breastfeeding in preterm infants [11]. Mothers are
recommended to initiate breast milk expression soon after the
delivery but there is no consensus as to how early this should be
done. In some studies it is recommended to start within the first
6 hours after delivery [12] whereas others suggest 24 hours [13]. A
recent randomised controlled trial found that the initiation of
breast milk expression within one hour, compared to six hours,
after delivery doubled the mothers volume of milk for the first
three weeks [14].
Skin-to-skin contact between the preterm infant and the
mother/parents is also shown to promote breastfeeding [15],
[16], [17], [18]. However, the effect of the timing of intermittent
skin-to-skin contact has not been investigated. Rooming-in of the
mother together with the infant in maternity units has shown to be
associated with better breastfeeding outcomes [19], but research
on the effect, on breastfeeding, of the admittance of mothers with
their infants to NICUs, is sparse [20].
When the preterm infant is ready to initiate breastfeeding the
use of a nipple shield is a possibility. In general nipple shields are
not recommended for term infants [21], but reports on the
advantages of nipple shield use for preterm infants came 1317
years ago [22], [23] and, against this background, nipple shields
have been widely recommended for preterm infants [24], [25]. A
recent literature review concludes that current published research
does not provide evidence for the safety or effectiveness of
contemporary nipple shield use for either preterm or non-preterm
infants [26].
Measurement of milk intake by weighing the infant immediately
before and after a breastfeeding session called test-weighing
has been recommended for preterm infants [24], [27], [28] and
half of the Danish Neonatal Intensive Care Units (NICUs) use the
test-weighing procedure by routine [2].
The use of a pacifier in preterm infants has been shown to
relieve pain and reduce stress in the absence of the mother [29],
[30], and is therefore widely used for preterm infants, although the
use of a pacifier is not recommended for healthy newborns [21] as
it is associated with lower breastfeeding outcomes [31]. An
Australian randomised controlled trial of pacifier use in preterm
infants showed no significant difference between groups in
breastfeeding rates at discharge nor in breastfeeding duration
[32], and a Brazilian study found that no use of a pacifier
improved the likelihood of exclusive breastfeeding for preterm
infants at six months with a 1,7 factor [33].
Aim and Objectives
Our primary aim was to investigate the association between
early breast milk expression, early initiation of skin-to-skin contact,
rooming-in, nipple shield use, test-weighing, and pacifier use, and
the establishment of exclusive breastfeeding at discharge, as well as
at a predefined interval after discharge, in order to gain more
evidence on which to base guidelines for mothers to preterm
infants in the NICU.
Materials and Methods
Ethics Statement
The study was conducted in accordance with the Declaration of
Helsinki [34] and approved by the Danish Data Protection Agency
(j.nr. 2009-41-4024); surveys do not, by Danish law, need to be
approved by the Biomedical Research Ethics Committee.
The mothers of the preterm infants gave written informed
consent for participation.
Design
The study was part of a prospective survey of a national Danish
cohort of preterm infants based on questionnaires and structured
telephone interviews conducted from September 2009 to Decem-
ber 2011.
Setting
Denmark, with its 5.5 million inhabitants, has about 63,000
births per year, seven per cent of which are premature births.
Denmark has public health care and all citizens can be treated in
public hospitals free of charge. In connection with the birth,
parents in Denmark are entitled to paid parental leave. Mothers
have paid leave for a minimum of four weeks before delivery and
up to 10.5 months after delivery, of which 7.5 can be shared with
the father/partner. If the infant stays in hospital due to illness and/
or prematurity, the leave is extended with the length of the hospital
stay by a maximum of three months. Partners have two weeks
leave following birth. An extra year of parental leave is possible
without payment [35].
Except for many of the late preterm infants (GA 35 36 weeks),
who do not need neonatal care, most of the preterm infants are
admitted to one of Denmarks 19 NICUs, where they are
hospitalised until breastfeeding is established (or exclusive
breastfeeding is given up, and mixed feeding or bottle feeding is
established) [2].
One of the NICUs provides low intensive care, 14 provide
medium intensive care, and four provide high intensive care [2].
Instruments
Based on a review of the literature and a National Expert Panel,
three study-specific questionnaires were developed to be answered
by the mother. The expert panel consisted of eight neonatal
nurses, with 1020 years each of experience in the breastfeeding of
preterm infants. Four of them were International Board Certified
Lactation Consultants (IBCLCs); three of them had research
knowledge.
Questionnaire 1 (Q1) contained 38 questions including demo-
graphic questions about mother and infant, and questions about
breastfeeding plans, experiences and self-efficacy, initiation of
breast milk expression and skin-to-skin contact (Questionnaire S1).
Questionnaire 2 (Q2) contained 59 questions about breastfeed-
ing initiation and establishment, feeding method(s) at discharge,
breast milk expression, test-weighing, and the mothers perceived
support. There were also questions about the reasons for and
timing of the use of pacifiers, bottle-feeding and nipple shields
(Questionnaire S2).
Questionnaire 3 (Q3) contained 17 questions about the length of
exclusive, and any, breastfeeding, possible reasons for ceasing,
length of nipple shield use and breast milk expression, and
perceived breastfeeding problems (Questionnaire S3).
In total the questionnaires included 30 interval scale variables,
76 categorical variables and three open questions.
Q1 was answered by the mothers approximately one week after
delivery, and Q2 was answered by the mothers at the time of the
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infants discharge from NICU to home. Q3 was used for
structured telephone interviews at 1, 4, 6 and 12 months of
corrected age or until breastfeeding ceased, whichever occurred
first.
Pilot study
The three questionnaires were revised by two senior academic
experts and, thereafter, 21 mothers from five different Danish
NICUs tested the questionnaires for content and face validity. The
pilot study led to minor changes.
Participants and datacollection
All preterm infants, that is infants less than 37 gestational weeks
old [36], who were admitted to the participating departments from
1 September 2009 to 31 August 2010 in their first five days of life,
could participate in the study.
Infants were excluded if an interpreter was not available for the
mother, if they were discharged to maternity units before five days
of age, or if they died.
All departments in Denmark that, as a routine, take care of
preterm infants during breastfeeding establishment were invited to
participate in the study, which included 18 of the 19 NICUs, two
special care units and one childrens department. All 21 units
agreed to participation and, of these, 18 units adhered to the
project protocol. The factors leading to non-adherence to the
protocol were that less than two third of the eligible infants were
approached or that enrolment slowed down during the last
months. Telephone interviews and data entering were performed
by the units and the National Expert Panel in charge of the study.
The first author checked all the data and crosschecked the extreme
and misleading data with the original responses.
The data from the survey will be publicly available on request,
when all data has been analysed in the summer of 2015 and the
data has been transferred to the Danish Data Archive.
Outcomes
1) Exclusive breastfeeding at discharge was defined as the infant
feeding directly at and from the breast, and it was thereby not
equal to feeding the infant with breast milk from a bottle or other
device. Exclusive breastfeeding at discharge could include
medication and vitamins and, for a few infants, powder
fortification mixed with the mothers expressed milk (which for
this study was considered as medication), but not water, formula or
anything else. 2) Adequate duration of exclusive breastfeeding:
The Danish Health Boards recommendation for exclusive
breastfeeding in preterm infants was chosen as the outcome for
adequate duration, that is exclusive breastfeeding for four months
plus half of the period of time the infant was born before estimated
date of delivery [37]. For the regression analyses we used failure of
exclusive breastfeeding and inadequate duration of exclusive
breastfeeding so that an odds ratio (OR) lower than one would
present factors with a positive association to breastfeeding, and a
higher OR would present factors with a negative association to
breastfeeding, since the majority of Danish preterm infants are
breastfed [3].
Variables and predictive variables
In the logistic regression analyses both variables concerning the
infant and the mother that were known at birth and that were
expected to have associations with breastfeeding, and variables
reflecting the clinical practices that were used to establish or
facilitate breastfeeding were entered. The variables were GA, in
weeks, categorised in four groups: extremely preterm infants GA
2427, very preterm infants GA 2831, moderate preterm infants
GA 3234, and late preterm infants GA 3536; multiple births;
being small for gestational age (SGA) (defined as birth weight more
than two standard deviations (SD) smaller than expected
according to GA); the educational level of the mother (based on
years of school and education), categorised in three groups: high
(more than 16 years), intermediate (1416 years), and low (less
than 14 years); experience with breastfeeding, categorised into five
groups: first time mothers, mothers who had not breastfed
previous infants, previous breastfeeding of an infant exclusively
for less than a month, for 1 4 months, and for more than four
months; maternal smoking; and mode of delivery (Caesarean
section). The variables reflecting clinical practices were the
initiation of breast milk expression after delivery, categorised in
five groups: before six hours, 612 hours, 1224 hours, 24
48 hours, and later than 48 hours; first skin-to-skin contact before
six hours postpartum; admitting mother and infant together into
the NICU; nipple shield use during hospitalisation; test-weighing
the infant at most breastfeeding sessions during transition from
tube-feeding to breastfeeding; pacifier use during hospitalisation,
categorised in three groups: no use of a pacifier, minimizing the
use of a pacifier during breastfeeding transition, and the
unrestricted use of a pacifier.
One or more of the following practices could be regarded as
minimizing the use of a pacifier during the transition from tube-
feeding to breastfeeding: predominantly using the pacifier during
tube-feedings, painful or stressful events, predominantly using the
pacifier in the mothers absence, or removing the pacifier
completely.
Statistical Analyses
SPSS version 21.0 was used for statistical analyses. Failure of
exclusive breastfeeding at discharge was analysed by means of
logistic regression models, first the explanatory variables were
analysed in univariate models and second the explanatory
variables with a p-value of less than 0.1 were analysed
simultaneously in a multiple model. Logistic regression analyses
were performed with one infant per mother (to ensure that
mothers of twins did not count as double [38]; for multiple births,
the first born infant was included). The variables from the
multivariate model analysing failure of exclusive breastfeeding at
discharge were also used for analysing the associations with the
second outcome, that is inadequate duration of exclusive
breastfeeding, to see if associations persisted.
Descriptive statistics were used to present characteristics. The
normally distributed results are reported with mean and standard
deviation (SD); the remaining results are reported with median
and interquartile range (IQR) or percentages [38]. Pearsons Chi-
Square test was used to determine statistically significant
differences for nominal data. Values of p,0.05 were considered
statistically significant.
Results
Participant selection
Selections of participants are described in the flow chart (Figure
1). During the one year period 2,579 preterm infants were
admitted to the NICUs; of these 281 were excluded either because
an interpreter was not available for the mother (n = 42), the
infants were discharged to maternity units before five days of age
(n = 188), or had died (n = 51). Thus 2,298 infants were eligible
for inclusion. Of these, 1,664 infants participated with Q1, and
1,431 infants participated with both Q1 and Q2; an additional 57
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infants with Q1 but without Q2 were also approached through
structured telephone interviews, and primary and secondary
outcomes were obtained. There were 1,488 infants (65% of
eligible) available for primary outcome, 46% (n = 60/131) of the
extremely preterm infants, 65% of (n = 257/398) the very
preterm infants, 70% (n =688/984) of the moderate preterm
infants, and 62% (n = 483/785) of the late preterm infants (Table
1). For the secondary outcome, 1,470 infants were available, and
the remaining 18 infants were included in the analysis as not
fulfilling breastfeeding duration.
Of the participating infants 322 were transferred between the
neonatal units. The number of participating mothers was 1,221.
Significantly fewer of the extremely preterm infants eligible for
inclusion participated at discharge from NICU (p , 0.0001). Of
mothers participating with Q1, significantly more of those who did
not return Q2 had a lower level of education (p , 0.001).
Participant characteristics
The mothers had a mean age of 31 years (SD = 5), 93% were
of Danish/Scandinavian origin, 98% had planned to breastfeed,
96% lived with the infants father and 97% of the mothers
reported that their breastfeeding plans were supported by their
partner. Twenty-two per cent of the mothers had multiple births
(more twins than triplets), 36% of the infants were multiples,
almost all (98%) of the infants had had skin-to-skin contact with
the mother within the first week, and 99% of the infants had
initiated breastfeeding. Table 2 shows rates of different charac-
teristics in exclusive and non-exclusive breastfeeding groups.
Breastfeeding rates
At discharge, 68% of the infants were exclusively breastfed,
17% were partially breastfed, and 15% were not breastfed. Some
Figure 1. Flow chart. BF = breastfeeding, M = mothers, NICU = Neonatal Intensive Care Unit, PI = preterm infants, Q1 = Questionnaire 1, Q2 =
Questionnaire 2. *The four infants who died after inclusion were all twins, no mothers were lost due to infant death.
doi:10.1371/journal.pone.0089077.g001
Table 1. Gestational age groups and drop out.
Gestational age, weeks
23 27 28 31 32 34 35 36
N (%) n (%) n (%) n (%) n (%)
Eligible for inclusion 2298 (100) 131 (100) 398 (100) 984 (100) 785 (100)
Consented participation 1747 (76) 91 (69) 320 (80) 789 (80) 547 (70)
Breastfeeding outcomes 1488 (65) 60 (46) 257 (65) 688 (70) 483 (62)
N = total number, n = sub group numbers.
doi:10.1371/journal.pone.0089077.t001
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of the infants were fed with breast milk from bottles. Adding those
infants to the breastfed infants, 77% were exclusively breast milk
fed at discharge, 15% were partially breast milk fed, and eight per
cent were not fed breast milk at all at the time of discharge. Thirty-
one per cent were breastfed exclusively for the recommended
duration.
The exclusive breastfeeding rates at discharge varied signifi-
cantly between the participating units from 53 to 83% (p ,
0.0001), as did rates of nipple shield use from 35 to 67% (p ,
0.0001), pacifier use from 60 to 100% (p , 0.0001), and the use of
test-weighing from 0 to 87%(p .0.0001). Counting one infant per
mother, 76% of the infants who were test-weighed at most
breastfeeding sessions were exclusively breastfed at discharge
compared to 69% of the infants who were not test-weighed at most
breastfeeding sessions (p = 0.02). One month after discharge the
corresponding proportion was 59% and 57%, respectively, with no
statistically significant difference.
Breastfeeding at discharge
The univariate analyses showed that all the factors from the set
of variables, together with the gender of the infant, were
significantly associated with exclusive breastfeeding at discharge
(Table 3). The multivariate analysis showed that the following
characteristics were each independently associated with signifi-
cantly higher odds of failure of exclusive breastfeeding at
discharge: extremely preterm and very preterm infants, multiple
births (twins and triplets) and boys. Furthermore, infants to
mothers who had not breastfed previous infants or who smoked
had higher odds for failure of exclusive breastfeeding at discharge
(OR 5.6 (95% CI 2.0 15.9), and 2.2 (95% CI 1.4 3.7)
respectively).
A number of clinical practices were associated with a
significantly higher OR of failure of exclusive breastfeeding at
discharge (Figure 2). Infants using nipple shields had a 2.3-fold
increased risk. Delayed initiation of breast milk expression showed
Table 2. Proportions of infant and mother characteristics and clinical practices in exclusive and non-exclusive breastfeeding
groups.
Exclusive breastfeeding at discharge
(One infant per mother) Total n/N Yes % No %
Multiple births 263/1221 18 31 ****
SGA 191/1211 14 21 *
Boy 644/1221 51 58 *
Maternal education NS
High 403/1207 32 37
Intermediate 567/1207 47 48
Low 237/1207 21 16
Breastfeeding experience, lenght of excl. BF ****
. 4 months 196/1171 19 10
1 4 months 167/1171 14 15
, 1 month 21/1171 1 3
Not breastfed previous infants 27/1171 1 5
First-time mothers 760/1171 64 67
Maternal smoking 123/1210 8 15 ***
Mode of delivery, caesarean section 614/1219 48 57 **
Mother admitted together with infant to the NICU 344/1207 31 22 **
First breast milk expression **
, 6 hours pp 255/1183 23 19
6 12 hours pp 469/1183 41 38
12 24 hours pp 288/1183 25 24
24 48 hours pp 141/1183 11 15
. 48 hours pp 30/1183 2 5
Been skin-to-skin with mother within 6 hours pp 700/1217 61 48 ****
Nipple shield use 629/1160 49 66 ****
Pacifier use ****
No pacifier 132/1144 13 7
Minimizing use of a pacifier 337/1144 34 19
Unrestricted use 675/1144 53 73
Test-weighing at most breastfeedings 351/1160 32 25 *
* = p , 0,05, ** = p, 0,01, *** = p, 0,001, **** = p, 0,0001.
BF = breastfeeding, excl. = exclusive, n/N = number of infants or mothers with the characteristic/number of responses, NS = Non-significant, pp = postpartum, SGA
= Small for gestational age.
doi:10.1371/journal.pone.0089077.t002
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a dose-response effect: the later the initiation, the higher the risk
for failure to exclusively breastfeed at discharge, although only
initiation later than 48 hours postpartum reached significance
(OR 4.9 (95% CI 1.9 12.6)). Test-weighing the infant at most
breastfeeding sessions during transition from tube-feeding to
breastfeeding was associated with a lower risk (OR 0.6 (95% CI
0.4 0.8)) of failure to exclusively breastfeed at discharge and thus
positively related to exclusive breastfeeding. The same association
was seen for no use of a pacifier and for minimizing the use of a
pacifier during breastfeeding transition OR 0.6 (95% CI 0.3 1.0)
and 0.4 (95% CI 0.3 0.6) respectively.
The difference in exclusive breastfeeding rates between the
NICUs persisted when adjusting for infant and maternal
characteristics and clinical procedures (p = 0.001).
Duration of breastfeeding
Testing factors associated with adequate duration of exclusive
breastfeeding showed that multiple births and maternal smoking
had similar results with regards to exclusive breastfeeding at
discharge (Table 4). Neither gestational age groups nor the infants
gender were associated with adequate duration of exclusive
breastfeeding.
In addition, maternal education at either an intermediate or low
level was a risk factor. Compared to mothers who had breastfed a
Table 3. Odds for failure of exclusive breastfeeding at discharge from NICU to home.
(one infant per mother)
Unadjusted analyses
Adjusted analysis
(N = 1007)
Infant and mother characteristics N Prev. OR (95% CI) OR (95% CI)
Gestational age groups, GA 24 27 weeks 1221 4% 3.0 (1.7 5.5) *** 2.9 (1.3 6.4) **
GA 28 31 weeks 18% 1.6 (1.1 2.3) * 1.8 (1.1 2.9) *
GA 32 34 weeks 48% 1.0 (0.8 1.3) 1.0 (0.7 1.4)
GA 35 36 weeks (ref) 33% 1 1
Multiple birth 1221 22% 2.1 (1.6 2.9) **** 2.0 (1.4 2.9) ***
Small for gestational age 1211 16% 1.7 (1.2 2.3) ** 1.2 (0.8 1.9)
Gender, boys 1221 53% 1.4 (1.1 1.7) * 1.7 (1.3 2.3) **
Maternal education, high ( ref) 1207 20% 1 1
Intermediate 47% 1.4 (1.0 2.0) 1.3 (0.9 2.0)
Low 33% 1.5 (1.1 2.2) * 1.2 (0.8 1.9)
Breastfeeding experience, lenght of excl. BF 1171
.4 mo. (ref) 17% 1 1
1 4 months 14% 2.0 (1.2 3.3) ** 1.6 (0.9 2.9)
, 1 month 2% 4.3 (1.7 11.0) ** 2.7 (0.9 8.5)
Not breastfed previous infants 2% 8.1 (3.4 19.2) **** 5.6 (2.0 15.9) **
First time mothers 65% 2.0 (1.4 3.0) ** 1.4 (0.9 2.3)
Maternal smoking 1210 10% 1.9 (1.3 2.8) ** 2.2 (1.4 3.7) **
Mode of delivery, caesarean section 1219 50% 1.4 (1.1 1.8) ** 1.1 (0.8 1.5)
Breastfeeding practices
Mother admitted together with infant to the NICU 1207 29% 0.6 (0.5 0.9) ** 0.8 (0.6 1.2)
First breast milk expression, , 6 hours pp (ref) 1183 22% 1 1
6 12 hours pp 40% 1.1 (0.8 1.6) 1.0 (0.7 1.6)
12 24 hours pp 24% 1.2 (0.8 1.8) 1.1 (0.7 1.8)
24 48 hours pp 12% 1.7 (1.1 2.7) * 1.5 (0.8 2.6)
. 48 hours pp 3% 3.8 (1.8 8.3) ** 4.9 (1.9 12.6) **
Been skin-to-skin with mother within 6 hours pp 1217 58% 0.6 (0.5 0.8) **** 1.1 (0.8 1.6)
Nipple shield use 1160 54% 2.0 (1.5 2.6) **** 2.3 (1.6 3.2) ****
Pacifier use, no pacifier 1144 12% 0.4 (0.2 0.6) *** 0.6 (0.3 1.0) *
Minimizing use of a pacifier 30% 0.4 (0.3 0.6) **** 0.4 (0.3 0.6) ****
Unrestricted use of a pacifier (ref) 59% 1 1
Test-weighing at most breastfeeds 1160 30% 0.7 (0.5 0.9) * 0.6 (0.4 0.8) **
* = p , 0,05, ** = p, 0,01, *** = p, 0,001, **** = p, 0,0001.
BF = breastfeeding, CI = confidence interval, GA = Gestational age, N = Number included in unadjusted analyses, (N = 1007) = Number included in adjusted
analysis NICU = Neonatal Intensive Care Unit, OR =odds ratio, pp =post partum, prev = prevalence.
doi:10.1371/journal.pone.0089077.t003
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previous infant for more than four months, less or no breastfeeding
experience was associated with a higher OR for inadequate
breastfeeding duration.
As for clinical practices, the delayed initiation of breast milk
expression again showed a dose-response effect the later the
expression was initiated the higher the OR with initiation 12
24 hours and 24 48 hours postpartum reaching significance for
inadequate breastfeeding duration (OR 1.6 (95% CI 1.0 2.4) and
1.8 (95% CI 1.0 3.1), respectively) (Figure 3). Also, the use of
nipple shields was associated with a higher OR for inadequate
breastfeeding duration (OR 1.4 (95% CI 1.1 1.9)). The use of
test-weighing or the use of a pacifier were not significantly
associated with adequate breastfeeding duration.
Discussion
We presented data from a national cohort of preterm infants
and found a relatively high rate of exclusive breastfeeding at
discharge (68%) compared to 27 60% of preterm infants in US
and Scandinavian studies [3], [39], [40], [41], showing that it is
possible to establish exclusive breastfeeding in the majority of
preterm infants. The odds of breastfeeding failure at discharge
were inversely related to gestational age: the lower the gestational
age the higher the odds for breastfeeding failure at discharge, even
when we corrected for potential confounders such as multiple
births, mode of delivery, SES, and maternal smoking. The
association is not surprising and could be explained by an
increased risk of morbidity and a longer time where the infant is
admitted to the NICU. However, our data also showed that if the
mother were to succeed in the establishment of exclusive
breastfeeding at discharge the significant impact of gestational
age disappeared when the duration of exclusive breastfeeding was
the outcome. The mothers education is usually associated with
breastfeeding establishment and duration [3], [7], [9], [10], [42]
but in our study the association was only seen in connection to
breastfeeding duration. This was a surprising finding and could be
due to the NICUs ability to support less educated mothers during
hospitalisation.
The present study is the first to examine several different time
intervals of initiation of breast milk expression, and showed a dose-
response effect on both outcomes: the later the initiation the higher
the odds increasing from 1.0 to 4.9 for breastfeeding failure at
discharge and for inadequate breastfeeding duration. The 12
24 hours and 2448 hours intervals were significantly associated
with breastfeeding duration (p,0,05). For breastfeeding failure at
discharge we found a more significant association (p,0,01), but
with a later time interval (. 48 hours postpartum). The results
indicate that exclusive breastfeeding is not impossible if breast milk
expression is initiated later than 12 hours postpartum, but it seems
that initiating this even before six hours postpartum would be
helpful for mothers who want to breastfeed their preterm infant.
These results support other studies finding that breast milk
expression should be initiated at an early stage after the delivery
[12], [13], [14]. From another study we know that 89% of the
Danish NICUs would advise the mothers to initiate breast milk
expression within six hours after delivery [2], but only 22% of the
mothers did so. Even though our results could be biased by other
factors such as the mothers disease, we consider it reasonable to
recommend that breast milk expression should be initiated as soon
as possible.
The timing of initiation of skin-to-skin contact and the
admittance of the mother directly after delivery together with
the infant to the NICU did not show a significant association to
breastfeeding in the present study. Our study was not designed to
give definitive answers to whether or not these practices promote
breastfeeding and, furthermore, it should be emphasized that there
may be other benefits of these practices for the mother-infant
relationship than that of promoting breastfeeding. Skin-to-skin
contact has previously been positively associated with breastfeed-
ing preterm and non-preterm infants [15], [16], [17], [43], but
only one study of preterm infants demonstrated that the initiation
of continuous skin-to-skin contact before 24 hours postpartum was
positively associated with exclusive breastfeeding at six months of
age [19]. Most of the infants (98%) in the present study had skin-
to-skin contact during the NICU stay, and it seems that even if
Figure 2. Forest plot. BM expres. = Breast milk expression, h = hours, NICU = Neonatal Intensive Care Unit, pp = postpartum, ref = reference.
doi:10.1371/journal.pone.0089077.g002
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42% of the mothers were not able to have early skin-to-skin
contact with their preterm infants this was not an essential barrier
to the establishment of breastfeeding. On the other hand, it has
previously been shown that it is possible to establish skin-to-skin
contact even with extremely preterm infants [44], and although
there is no evidence that this promotes breastfeeding we find no
reason not to recommend this practice unless there are medical
reasons that oppose this.
We did not ask the 29% of mothers in the present study who
were admitted to the NICU directly after delivery together with
the infant, where in the NICU they had slept (next to the infant, or
in another room in the NICU), and we did not ask for how long
they had stayed in the NICU. Mothers, who were not admitted to
the NICU directly after delivery, were not asked if they were
admitted to the NICU later or for how long they could sleep in the
NICU. From a previous study we know that all Danish NICUs
offered the mothers rooming-in some days before discharge, and
in 42% of the NICUs the mother could have a bed in the NICU
when she was discharged from maternity ward [2]. Therefore, we
still lack knowledge of whether or not rooming-in for the infants
whole hospitalisation period (defined as sleeping together) is
associated with breastfeeding success for preterm infants, just as it
is for non-preterm infants [19]. A Swedish study found that
mothers separated from their newborn infants experienced
emotional strain and anxiety; they felt like they were outsiders,
and experienced a lack of control when the infant was admitted to
neonatal intensive care [45]. A Danish study found that the
possibility for rooming-in in a neonatal ward could help the
parents feel like a family and not just visitors to their own baby
[46]. For these reasons efforts should still be made to avoid
separating the mother and the preterm infant.
The use of a nipple shield has previously been described as a
facilitator of breastfeeding in preterm infants, but only in small
studies with 15 and 34 infants and no control groups [22], [23]. In
our study the use of nipple shields was negatively associated with
exclusive breastfeeding establishment and duration. Nipple shields
are often used to solve breastfeeding problems, some of the
problems may be hard to solve, even with a nipple shield, but the
huge variation in nipple shield use between the NICUs
hospitalising similar infants (3567% of discharged infants)
indicates that a nipple shield was not always used because of
severe latching problems. Thus, although our results could be
biased, they suggest that the use of nipple shields does not promote
breastfeeding in preterm infants, just as it does not promote
breastfeeding in non-preterm infants [26].
Test-weighing the infant at most breastfeeding sessions during
transition was, in the present study, protective to exclusive
breastfeeding at discharge, but had no association with breastfeed-
ing duration. Mothers of preterm infants are concerned about
their small infants getting enough milk and growing well, which
could be a reason why test-weighing seems to help establish
exclusive breastfeeding. The protective effect was eliminated
within one month of discharge, indicating that mothers using
test-weighing in the NICU ceased exclusive breastfeeding earlier
after discharge, when they could not measure the amount of milk
that their infant sucked. Earlier studies from Sweden show
contadictory results: One Swedish study comparing two units,
found no differences in breastfeeding outcome at discharge [47],
whereas another Swedish study using a quasi-experimental design
found that infants in the not test-weighing group were twice as
likely to fail exclusive breastfeeding at discharge [48], as was the
case in the present study. Test-weighing has previously been found
to be associated with a shorter duration of exclusive breastfeeding
for term infants [49].
Pacifier use is also controversial. The multivariate analysis
showed that no use of a pacifier and the minimization of the use of
a pacifier during breastfeeding transition were both positively
associated with exclusive breastfeeding at discharge, but not
associated with breastfeeding duration. A Brazilian study supports
that not using a pacifier at all is positive for exclusive breastfeeding
of preterm infants [33], as it is for term infants [31]. To our
knowledge, minimizing the use of a pacifier during breastfeeding
transition has not previously been studied for preterm infants, but
could be a useful intervention for the many preterm infants using
pacifiers during hospitalisation.
Table 4. Odds for inadequate duration of exclusive
breastfeeding.
(one infant per mother)
Adjusted analysis
(N = 1007)
Infant and mother characteristics OR (95% CI)
Gestational age groups, GA 24 27 weeks 1.6 (0.7 3.7)
GA 28 31 weeks 1.4 (0.9 2.2)
GA 32 34 weeks 1.2 (0.9 1.7)
GA 35 36 weeks (ref) 1
Multiple birth 2.4 (1.6 3.6) ****
Small for gestational age 1.2 (0.8 1.7)
Gender, boys 1.1 (0.8 1.5)
Maternal education, high ( ref) 1
Intermediate 1.6 (1.1 2.3) **
Low 2.6 (1.7 3.9) ****
Breastfeeding experience, lenght of excl. BF, .4 mo. (ref)1
1 4 months 3.5 (2.1 5.9) ****
, 1 month 11.1 (2.2 54.7) **
Not breastfed previous infants 8.7 (2.3 32.2) **
First time mothers 2.7 (1.8 4.0) ****
Maternal smoking 3.4 (1.8 6.5) ***
Mode of delivery, caesarean section 0.9 (0.7 1.3)
Breastfeeding practices
Mother admitted together with infant to the NICU 0.8 (0.6 1.1)
First breast milk expression, , 6 hours pp (ref) 1
6 12 hours pp 1.2 (0.8 1.7)
12 24 hours pp 1.6 (1.0 2.4) *
24 48 hours pp 1.8 (1.0 3.1) *
. 48 hours pp 2.1 (0.8 5.6)
Been skin-to-skin with mother within 6 hours pp 1.3 (0.9 1.8)
Nipple shield use 1.4 (1.1 1.9) *
Pacifier use, no pacifier 0.8 (0.5 1.3)
Minimizing use of a pacifier 0.8 (0.6 1.1)
Unrestricted use of a pacifier (ref) 1
Test-weighing at most breastfeeds 0.9 (0.7 1.2)
* = p , 0,05, ** = p, 0,01, *** = p, 0,001, **** = p, 0,0001.
BF = breastfeeding, CI = confidence interval, GA = Gestational age, (N =
1007) = Number included in adjusted analysis NICU = Neonatal Intensive Care
Unit, OR =odds ratio, pp =post partum.
doi:10.1371/journal.pone.0089077.t004
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Strengths and limitations
The strengths of the present study are: the large number of
participating preterm infants and mothers, the fact that the study is
national, and the carrying out of repeated structured telephone
interviews so as to reduce recall bias.
It is a clear limitation that our observational study was not
designed to establish cause and effect relationships. However, a
large study like ours provides important evidence from the daily
clinic that supports, or questions, the recommendations based on
data from smaller studies. Another limitation is that two out of four
high intensive neonatal units did not enrol mother-infant pairs,
and although mostly all infants were transferred to participating
NICUs, more of the infants with the lowest gestational age were
not approached. That could be because the infants were more
than a month old at transfer, which could be a barrier for asking
the mothers to participate in a study that optimally should have
begun a week after the infants birth. It is also known that
participants with poorer health outcomes are more reluctant to
participate in surveys and more often drop out from cohorts [50].
Also, the high drop-out rate of extremely preterm infants could
indicate that they are at an even greater risk for not being
exclusively breastfed than this study could show. The higher drop-
out rate of less educated mothers before discharge, could affect the
result of education having no association to exclusive breastfeeding
at discharge.
The structured telephone interviews, conducted by NICU
nurses experienced in breastfeeding, could serve as an interven-
tion, where the mothers could get answers to their breastfeeding
questions, as there were no limitations in the nurses answers to the
mothers questions. Results in the present study of late preterm
infants cannot be generalised to all late preterm infants, as late
preterm infants admitted to NICUs have more health problems
than late preterm infants cared for in maternity units. During the
study period the Danish hospitals went through reductions in
hospital staff influencing most of the participating units, resulting
in some units not having the time for telephone interviews and
entering data.
Conclusions
Mothers of preterm infants should be guided to initiation of
early breast milk expression before 12 hours postpartum, as this
may result in better breastfeeding outcomes. Our data also suggest
that the use of nipple shields should be restricted for preterm
infants. Use of test-weighing and minimizing the use of a pacifier
during breastfeeding establishment may promote exclusive
breastfeeding, but more research is needed regarding adequate
support to the mother when test-weighing is ceased, as more of
these mothers ceased exclusive breastfeeding early after discharge.
In order to increase exclusive breastfeeding rates for preterm
infants, special breastfeeding support and guidance should be
given to first-time mothers, smokers, mothers with a lower level of
education, mothers of infants younger than 32 gestational weeks,
and mothers of twins and triplets.
Supporting Information
Questionnaire S1 Breastfeeding survey. Questionnaire 1 for
the babys mother at the beginning of the babys hospitalization.
(PDF)
Questionnaire S2 Breastfeeding survey. Questionnaire 2 for
the babys mother at the babys discharge.
(PDF)
Questionnaire S3 Breastfeeding survey. Questionnaire 3 used
for telephone interviews with the babys mother.
(PDF)
Acknowledgments
The authors wish to thank the contact persons and nurse leaders in the
Danish NICUs participating in the study for their practical support in the
study in a time of limited resources, as well as the mothers and infants who
participated in the study.
Figure 3. Forest plot. BM expres. = Breast milk expression, h = hours, NICU = Neonatal Intensive Care Unit, pp = postpartum, ref = reference.
doi:10.1371/journal.pone.0089077.g003
Exclusive Breastfeeding of Preterm Infants
PLOS ONE | www.plosone.org 9 February 2014 | Volume 9 | Issue 2 | e89077
Author Contributions
Conceived and designed the experiments: RM SB KH AF AK IS HK.
Performed the experiments: RM SB KH AF AK IS. Analyzed the data:
RM BMH. Contributed reagents/materials/analysis tools: RM SB KH AF
AK IS. Wrote the paper: RM BMH IH. Interpretation of results: RM
BMH HK SB KH AF AK IS IH. Revision of manuscript: RM BMH HK
SB KH AF AK IS IH.
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